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Echium L. (Boraginaceae) (Speciation/Selection/Perennial Growth/Woodiness/Founding Populations) UTA-REGINA B6HLE*, HARTMUT H

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Echium L. (Boraginaceae) (Speciation/Selection/Perennial Growth/Woodiness/Founding Populations) UTA-REGINA B6HLE*, HARTMUT H Proc. Natl. Acad. Sci. USA Vol. 93, pp. 11740-11745, October 1996 Evolution Island colonization and evolution of the insular woody habit in Echium L. (Boraginaceae) (speciation/selection/perennial growth/woodiness/founding populations) UTA-REGINA B6HLE*, HARTMUT H. HILGER*, AND WILLIAM F. MARTINtt *Institut fur Systematische Botanik und Pflanzengeographie, Freie Universitat Berlin, Altensteinstrasse 6, D-14195 Berlin-Dahlem, Germany; and tInstitut fur Genetik, Technische Universitat Braunschweig, Spielmannstrasse 7, D-38023 Braunschweig, Germany Communicated by Peter H. Raven, Missouri Botanical Garden, St. Louis, MO, August 1, 1996 (received for review March 19, 1996) ABSTRACT Numerous island-inhabiting species of pre- mism is strict; no island species occur naturally in continental dominantly herbaceous angiosperm genera are woody shrubs floras and vice versa. Second, insular woodiness is very or trees. Such "insular woodiness" is strongly manifested in strongly pronounced in the genus; all but two of the island the genus Echium, in which the continental species of circum- species (Echium bonnetii and Echium pitardii) are woody mediterranean distribution are herbaceous, whereas endemic perennials, whereas the continental species are annual to species of islands along the Atlantic coast of north Africa are perennial herbs (or very rarely subshrubs). Third, the ages of woody perennial shrubs. The history of37 Echium species was the islands on which the woody species occur are known traced with 70 kb of noncoding DNA determined from both (9-14), so that the evolutionary process can be correlated to chloroplast and nuclear genomes. In all, 239 polymorphic geologic time. Island species of Echium reveal a degree of positions with 137 informative sites, in addition to 27 infor- morphological diversity comparable to that found in the mative indels, were found. Island-dwelling Echium species are remaining ("2000) species of the family. This is reflected in shown to descend from herbaceous continental ancestors via woody habits of the perennial island species: candelabra shrubs a single island colonization event that occurred <20 million and monocarpic rosette trees, the large vegetative rosettes of years ago. Founding colonization appears to have taken place which are formed over several vegetation periods and produce on the Canary Islands, from which the Madeira and Cape single inflorescences of several thousand flowers prior to Verde archipelagos were invaded. Colonization of island hab- fruiting and death. The herbaceous continental species reveal itats correlates with a recent origin of perennial woodiness much less diversity in form and preferentially inbreed, whereas from herbaceous habit and was furthermore accompanied by the island species are preferential outbreeders (15, 16). The intense speciation, which brought forth remarkable diversity Macaronesian species inhabit virtually all characteristic vegeta- offorms among contemporary island endemics. We argue that tion zones of the islands: coastal rocks, cliffs, semidesert habitats, the origin of insular woodiness involved response to counter- the laurel forest region, and the volcanic subalpine zone. selection of inbreeding depression in founding island colonies. Wishing to better understand the evolution of perennial woody habits in Echium and the phylogenetic process behind That island-dwelling species of numerous, predominantly her- diversity of its island species, we have inferred the phylogeny baceous genera of flowering plants tend to exhibit a perennial of 37 Echium species-including most of the island inhabit- and woody growth form was evident to Darwin (1), Wallace ants-and four outgroup representatives by amplifying, se- (2), and many others since. Carlquist (3) coined the term quencing, and analyzing noncoding DNA regions from both "insular woodiness" to designate the phenomenon (which also their chloroplast and nuclear genomes. The data reveal that is observed in highland biota; refs. 4 and 5) and found evidence perennial, woody Macaronesian Echium species arose <20 that wood morphology and development in such plants differ million years ago (mya) from herbaceous continental anteced- from that of common woody tissues. The insular woody habit ants and that all contemporary island dwellers can be traced to occurs in several angiosperm families, among them Boragi- a single founding colonization event emanating from conti- naceae, Asteraceae, Campanulaceae, Lobeliaceae, and Eu- nental forms. Evidence that the origin of insular woodiness in phorbiaceae, and was suggested to have evolved several times Echium was crucial to colonization-related diversification of independently from the herbaceous as an adaptation to cli- island forms supports and extends Wallace's suggestion (2) matic (primarily release from seasonality) and other factors that reproduction rather than adaptation is ultimately causal to (e.g., absence of large herbivores; ref. 3). According to the perennial woody habit in island species. opposing relict hypothesis, which draws support from mor- phological, cytological, and paleogeographical data, the woody habit of island forms is considered ancestral to the herbaceous MATERIALS AND METHODS habit (6-8). Whereas polarity of evolution for perennial Twenty-four of the 27 island Echium species, in addition to 13 woodiness in island species has been heavily debated (2-8), continental species predominantly of west Mediterranean problems concerning the underlying evolutionary mechanisms flora and four confamilial outgroup representatives, were through which it arose have remained largely intractable. investigated (Table 1). The outgroup representatives investi- An excellent case example of insular woodiness (Fig. 1) is gated were L. fruticosus Buek, Cerinthe minor L., Cerinthe found in Echium L. (Boraginaceae). Its size and distribution major L., and Lithodora diffusa (Lag.) I. M. Johnston. Material are particularly well-suited to study the phenomenon in several was collected either in the field or from various botanical respects. First, 27 species of Echium are endemic to the gardens and herbariums. All details of sources for all individ- Canary, Madeira, and Cape Verde archipelagos of the Mac- ual accessions are available from the authors ronesian islanids, whereas the remaining ("30) congeners are upon request. found in circummediterranean-west Asian floras. Their ende- Abbreviations: cpDNA, chloroplast DNA; mya, million years ago. Data deposition: The sequences reported in this paper have been The publication costs of tlfis lircle were defrayed in part by page charge deposited in the GenBank data base (accession nos. L43165-L43324). payment. This article must therefore be hereby marked "advertisement" in ITo whom reprint requests should be addressed. e-mail: w.martin@ accordance with 18 U.S.C. §1734 solely to indicate this fact. tu-bs.de. 11740 Downloaded by guest on September 29, 2021 EVOlUtiOn: BOh1e et al. Proc. Natl. Acad. Sci. USA 93 (1996) 11741 trnLUAA-trnFGAA Spacer Continental species ... TTACACAAGTCTTGTATGATA... Island species ...TTACA---------TATGATA... trnLUAA Intron Continental species ...GACT-----GCTTTGG... except E. sabulicola ... GCCTGCTTTGCTTTGG... E. parviflorum ... GCCTGCTTTGCTTTGG... Island species ... GACTGCTTTGCTTTGG... FIG. 2. Phylogenetic distribution of two indels found in Echium DNA sequences. informative indels (alignment available from the authors upon request). The trnLuAA intron shows least variability among all regions investigated (Table 2); average divergence of the nuclear ITS1 is 4- to 20-fold higher than that of the cpDNA spacers, depending on the species group under consideration (Table 2). Nuclear divergence within the island species is remarkably lower than within their continental congeners, ranging from 0.02-0.2% to 1.9% for cpDNA markers and ITS1, respectively (Table 2). We found several length polymorphisms (indels) in the chloroplast data set, two of which are either unique to the island species investigated or to the latter and two of the continental species, E. parviflorum and E. sabulicola (Fig. 2). Neighbor-joining and parsimony analyses of the combined FIG. 1. Echium creticum (Left) and Echium simplex (Right), rep- resentatives of the herbaceous continental and woody island species, data set of all four markers (Fig. 3) are totally consistent with respectively, found in this genus of circummediterranean and Maca- the indel distribution, providing unequivocal support for the ronesian (Canary, Madeira, and Cape Verde archipelagos) distribu- common descent of all island species investigated. Within the tion. E. creticum is annual to biennial, whereas E. simplex, an endemic continental species, the two coastal plants E. parviflorum and of the Anaga mountains (Tenerife), is a monocarpic rosette tree-i.e., E. sabulicola are more closely related to the Macaronesian forms a perennial vegetative rosette and flowers only once in life, species than to continental relatives, and represent the sister producing several thousand propagules and dies. group to the former. L. fruticosus was originally studied as an outgroup representative, since morphological evidence had DNA was isolated from leaf material (fresh, dried, or pre- suggested that this South African genus is closely related to served in 70% ethanol) as described (21), extracted with Echium. Yet L. fruticosus and all other members of that genus phenol/chloroform, and purified by ultrafiltration in Microcon investigated so far proved to be ingroups (unpublished
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